Culturable bacteria from two Portuguese salterns: diversity and bioactive potential

  • Eduarda AlmeidaEmail author
  • Teresa Vale Dias
  • Gonçalo Ferraz
  • Maria F. Carvalho
  • Olga M. Lage
Original Paper


Salterns are extreme environments, where the high salt concentration is the main limitation to microbial growth, along with solar radiation, temperature and pH. These selective pressures might lead to the acquisition of unique genetic adaptations that can manifest in the production of interesting natural products. The present study aimed at obtaining the culturable microbial diversity from two Portuguese salterns located in different geographic regions. A total of 190 isolates were retrieved and identified as belonging to 30 genera distributed among 4 phyla—Firmicutes, Proteobacteria, Actinobacteria and Bacteroidetes. Specifically, members of the genus Bacillus were the most frequently isolated from both salterns and all actinobacterial isolates belong to the rare members of this group. The molecular screening of NRPS and PKS-I genes allowed the detection of 38 isolates presenting PKS-I, 25 isolates presenting NRPS and 23 isolates presenting both types of biosynthetic genes. Sequencing of randomly selected amplicons revealed similarity with known PKS-I and NRPS genes or non-annotated hypothetical proteins. This study is the first contribution on the culturable bacterial diversity of Portuguese salterns and on their bioactive potential. Ultimately, these findings provide a novel contribution to improve the understanding on the microbial diversity of salterns.


Salterns Bacterial isolation Diversity Bioactive potential 



The authors thank national funds provided by Fundação para a Ciência e Tecnologia (FCT; Foundation for Science and Technology) at Portugal, and European Regional Development Fund (ERDF) and COMPETE under the Project INNOVMAR—Innovation and Sustainability in the Management and Exploitation of Marine Resources, reference NORTE-01-0145-FEDER-000035, Research Line NOVELMAR. This work was also financed by the Strategic Funding UID/Multi/04423/2019 through national funds provided by FCT and ERDF, in the framework of the programme PT2020. EA thanks FCT for the Ph.D. Grant SFRH/BD/125527/2016. M.F. Carvalho wishes to acknowledge CEEC program supported by FCT (CEECIND/02968/2017), Fundo Social Europeu and Programa Operacional Potencial Humano.

Author contributions

EA wrote the paper, collected samples, performed the experiments. TVD and GF helped on the experiments. MFC and OML collected samples and contributed for paper’s writing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

No human neither animals were used on this study. So, no need to report informed consent.

Supplementary material

10482_2019_1356_MOESM1_ESM.tif (20 kb)
Figure S1Mao’s Tau rarefaction curve associated with Aveiro and Olhão salterns’ bacterial communities and representing the species accumulation (TIFF 20 kb)
10482_2019_1356_MOESM2_ESM.xlsx (28 kb)
Table S1Overall information about salterns isolates including isolation conditions, identification on EzBioCloud database and corresponding similarity score, and PKS-I and NRPS PCR results (XLSX 28 kb)


  1. AlMatar M, Eldeeb M, Makky EA et al (2017) Are there any other compounds isolated from Dermacoccus spp. at all? Curr Microbiol 74:132–144. CrossRefPubMedGoogle Scholar
  2. Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  3. Amoutzias GD, Chaliotis A, Mossialos D (2016) Discovery strategies of bioactive compounds synthesized by nonribosomal peptide synthetases and type-I polyketide synthases derived from marine microbiomes. Mar Drugs 14:80. CrossRefPubMedCentralGoogle Scholar
  4. Antón J, Rosselló-Mora R, Rodríguez-Valera F, Amann R (2000) Extremely halophilic bacteria in crystallizer ponds from solar salterns. Appl Environ Microbiol 66:3052–3057. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Azman A-S, Othman I, Velu SS et al (2015) Mangrove rare actinobacteria: taxonomy, natural compound, and discovery of bioactivity. Front Microbiol 6:856. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Baati H, Amdouni R, Gharsallah N et al (2010) Isolation and characterization of moderately halophilic bacteria from Tunisian solar saltern. Curr Microbiol 60:157–161. CrossRefPubMedGoogle Scholar
  7. Ballav S, Kerkar S, Thomas S, Augustine N (2015) Halophilic and halotolerant actinomycetes from a marine saltern of Goa, India producing anti-bacterial metabolites. J Biosci Bioeng 119:323–330. CrossRefPubMedGoogle Scholar
  8. Baumann L, Baumann P, Mandel M, Allen RD (1972) Taxonomy of aerobic marine Eubacteria. J Bacteriol 110:402–429PubMedPubMedCentralGoogle Scholar
  9. Benlloch S, López-López A, Casamayor EO et al (2002) Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. Environ Microbiol 4:349–360. CrossRefPubMedGoogle Scholar
  10. Benson DA, Karsch-Mizrachi I, Lipman DJ et al (2005) GenBank. Nucleic Acids Res 33:D34–D38. CrossRefPubMedGoogle Scholar
  11. Berendonk TU, Manaia CM, Merlin C et al (2015) Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol 13:310–317. CrossRefPubMedGoogle Scholar
  12. Bibi F, Strobel GA, Naseer MI et al (2018) Halophytes-associated endophytic and rhizospheric bacteria: diversity, antagonism and metabolite production. Biocontrol Sci Technol 28:192–213. CrossRefGoogle Scholar
  13. Blunt JW, Copp BR, Keyzers RA et al (2015) Marine natural products. Nat Prod Rep 32:116–211. CrossRefPubMedGoogle Scholar
  14. Borsodi AK, Kiss RI, Cech G et al (2010) Diversity and activity of cultivable aerobic planktonic bacteria of a saline lake located in Sovata, Romania. Folia Microbiol (Praha) 55:461–466CrossRefGoogle Scholar
  15. Bowman JP (2016) Salegentibacter. In: Bergey’s Manual of systematics of archaea and bacteria. pp 1–11.
  16. Bruns A, Berthe-Corti L (2015) Muricauda. In: Bergey’s manual of systematics of archaea and bacteria. pp 1–8.
  17. Cane DE, Walsh CT (1999) The parallel and convergent universes of polyketide synthases and nonribosomal peptide synthetases. Chem Biol 6:R319–R325CrossRefGoogle Scholar
  18. Challinor VL, Bode HB (2015) Bioactive natural products from novel microbial sources. Ann N Y Acad Sci 1354:82–97. CrossRefPubMedGoogle Scholar
  19. Chen L, Wang G, Bu T et al (2010) Phylogenetic analysis and screening of antimicrobial and cytotoxic activities of moderately halophilic bacteria isolated from the Weihai Solar Saltern (China). World J Microbiol Biotechnol 26:879–888. CrossRefGoogle Scholar
  20. Çınar S, Mutlu MB (2016) Comparative analysis of prokaryotic diversity in solar salterns in eastern Anatolia (Turkey). Extremophiles 20:589–601. CrossRefPubMedGoogle Scholar
  21. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727CrossRefGoogle Scholar
  22. Di Meglio L, Santos F, Gomariz M et al (2016) Seasonal dynamics of extremely halophilic microbial communities in three Argentinian salterns. FEMS Microbiol Ecol 92:fiw184. CrossRefPubMedGoogle Scholar
  23. Díaz-Cárdenas C, Cantillo A, Rojas LY et al (2017) Microbial diversity of saline environments: searching for cytotoxic activities. AMB Express 7:223. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Donadio S, Monciardini P, Sosio M (2007) Polyketide synthases and nonribosomal peptide synthetases: the emerging view from bacterial genomics. Nat Prod Rep 24:1073–1109. CrossRefPubMedGoogle Scholar
  25. Fickers P (2012) Antibiotic compounds from Bacillus: why are they so amazing? Am J Biochem Biotechnol 8:38–43CrossRefGoogle Scholar
  26. Filker S, Gimmler A, Dunthorn M et al (2015) Deep sequencing uncovers protistan plankton diversity in the Portuguese Ria Formosa solar saltern ponds. Extremophiles 19:283–295. CrossRefPubMedGoogle Scholar
  27. Fleming A (1929) On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. Br J Exp Pathol 10:226–236PubMedCentralGoogle Scholar
  28. Fleming A (1944) The discovery of penicillin. Br Med Bull 2:4–5CrossRefGoogle Scholar
  29. Ghai R, Pašić L, Fernández AB et al (2011) New abundant microbial groups in aquatic hypersaline environments. Sci Rep 1:135. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gontang EA, Gaudêncio SP, Fenical W, Jensen PR (2010) Sequence-based analysis of secondary-metabolite biosynthesis in marine Actinobacteria. Appl Environ Microbiol 76:2487–2499. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Graça AP, Bondoso J, Gaspar H et al (2013) Antimicrobial activity of heterotrophic bacterial communities from the marine sponge Erylus discophorus (Astrophorida, Geodiidae). PLoS ONE 8:e78992. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Graça AP, Viana F, Bondoso J et al (2015) The antimicrobial activity of heterotrophic bacteria isolated from the marine sponge Erylus deficiens (Astrophorida, Geodiidae). Front Microbiol 6:389. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Groth I, Schumann P, Schütze B et al (2002) Knoellia sinensis gen. nov., sp. nov. and Knoellia subterranea sp. nov., two novel actinobacteria isolated from a cave. Int J Syst Evol Microbiol 52:77–84CrossRefGoogle Scholar
  34. Grubbs KJ, Bleich RM, Maria KCS et al (2017) Large-scale bioinformatics analysis of Bacillus genomes uncovers conserved roles of natural products in bacterial physiology. Mol Biol Physiol 2:e00040-17Google Scholar
  35. Haller CM, Rölleke S, Vybiral D et al (1999) Investigation of 0.2 µm filterable bacteria from the Western Mediterranean Sea using a molecular approach: dominance of potential starvation forms. FEMS Microbiol Ecol 31:153–161Google Scholar
  36. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9Google Scholar
  37. Han S-B, Yu Y-H, Ju Z et al (2018) Rhodohalobacter barkolensis sp. nov., isolated from a saline lake and emended description of the genus Rhodohalobacter. Int J Syst Evol Microbiol 68:1949–1954CrossRefGoogle Scholar
  38. Harwood CR, Mouillon J-M, Pohl S, Arnau J (2018) Secondary metabolite production and the safety of industrially important members of the Bacillus subtilis group. FEMS Microbiol Rev 42:721–738. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hezbri K, Nouioui I, Rohde M et al (2017) Blastococcus colisei sp. nov, isolated from an archaeological amphitheatre. Antonie Van Leeuwenhoek 110:339–346. CrossRefPubMedGoogle Scholar
  40. Hezbri K, Nouioui I, Rohde M et al (2018) Blastococcus xanthinilyticus sp. nov., isolated from monument. Int J Syst Evol Microbiol 68:1177–1183CrossRefGoogle Scholar
  41. Hibbing ME, Fuqua C, Parsek MR, Peterson SB (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8:15–25. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Hopwood DA (2007) How do antibiotic-producing bacteria ensure their self-resistance before antibiotic biosynthesis incapacitates them? Mol Microbiol 63:937–940. CrossRefPubMedGoogle Scholar
  43. Imada C (2013) Treasure hunting for useful microorganisms in the marine environment. In: Kim S (ed) Marine microbiology: bioactive compounds and biotechnological applications, 1st edn. Wiley, Hoboken, pp 21–31CrossRefGoogle Scholar
  44. Jose PA, Jebakumar SRD (2013) Diverse Actinomycetes from Indian coastal solar salterns—a resource for antimicrobial screening. Jounal Pure Appl Microbiol 7:2569–2575Google Scholar
  45. Kamat T, Kerkar S (2011) Bacteria from salt pans: a potential resource of antibacterial metabolites. Recent Res Sci Technol 3:46–52Google Scholar
  46. Kambourova M, Tomova I, Boyadzhieva I et al (2017) Phylogenetic analysis of the bacterial community in a crystallizer pond, Pomorie salterns, Bulgaria. Biotechnol Biotechnol Equip 31:325–332. CrossRefGoogle Scholar
  47. Kapley A, Tanksale H, Sagarkar S et al (2015) Antimicrobial activity of Alcaligenes sp. HPC 1271 against multidrug resistant bacteria. Funct Integr Genom 16:57–65. CrossRefGoogle Scholar
  48. Kennedy J, Baker P, Piper C et al (2009) Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar Biotechnol 11:384–396. CrossRefPubMedGoogle Scholar
  49. Kim TK, Garson MJ, Fuerst JA (2005) Marine actinomycetes related to the “Salinospora” group from the great barrier reef sponge Pseudoceratina clavata. Environ Microbiol 7:509–518. CrossRefPubMedGoogle Scholar
  50. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Labrenz M, Collins MD, Lawson PA et al (1999) Roseovarius tolerans gen. nov., sp. nov., a budding bacterium with variable bacteriochlorophyll a production from hypersaline Ekho Lake. Int J Syst Bacteriol 49:137–147CrossRefGoogle Scholar
  52. Lage OM, Bondoso J (2011) Planctomycetes diversity associated with macroalgae. FEMS Microbiol Ecol 78:366–375. CrossRefPubMedGoogle Scholar
  53. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
  54. Lee SD (2006) Blastococcus jejuensis sp. nov., an actinomycete from beach sediment, and emended description of the genus Blastococcus Ahrens and Moll 1970. Int J Syst Evol Microbiol 56:2391–2396. CrossRefPubMedGoogle Scholar
  55. Lee J-S, Lim J-M, Lee KC et al (2006) Virgibacillus koreensis sp. nov., a novel bacterium from a salt field, and transfer of Virgibacillus picturae to the genus Oceanobacillus as Oceanobacillus picturae comb. nov. with emended descriptions. Int J Syst Evol Microbiol 56:251–257. CrossRefPubMedGoogle Scholar
  56. Lee DW, Lee H, Kwon B-O et al (2018) Blastococcus litoris sp. nov., isolated from sea-tidal flat sediment. Int J Syst Evol Microbiol 68:3435–3440CrossRefGoogle Scholar
  57. Machado H, Sonnenschein EC, Melchiorsen J, Gram L (2015) Genome mining reveals unlocked bioactive potential of marine Gram-negative bacteria. BMC Genom 16:158. CrossRefGoogle Scholar
  58. Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902. CrossRefPubMedGoogle Scholar
  59. Mizuno CM, Kimes NE, López-Pérez M et al (2013) A hybrid NRPS-PKS gene cluster related to the bleomycin family of antitumor antibiotics in Alteromonas macleodii strains. PLoS ONE 8:e76021. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Muramatsu Y, Uchino Y, Kasai H et al (2007) Ruegeria mobilis sp. nov., a member of the Alphaproteobacteria isolated in Japan and Palau. Int J Syst Evol Microbiol 57:1304–1309. CrossRefPubMedGoogle Scholar
  61. Neilan BA, Dittmann E, Rouhiainen L et al (1999) Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. J Bacteriol 181:4089–4097. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Nespoli CR (2009) Characterization of extreme halophilic prokaryotic consortia of a traditional solar saltern in Olhão. Universidade do Algarve, Algarve (Portugal)Google Scholar
  63. Newman DJ, Cragg GM (2016) Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79:629–661. CrossRefPubMedGoogle Scholar
  64. Noar RD, Daub ME (2016) Bioinformatics prediction of polyketide synthase gene clusters from Mycosphaerella fijiensis. PLoS ONE 11:e0158471. CrossRefPubMedPubMedCentralGoogle Scholar
  65. Oren A (2015) Halophilic microbial communities and their environments. Curr Opin Biotechnol 33:119–124. CrossRefPubMedGoogle Scholar
  66. Oren A, Rodríguez-Valera F (2001) The contribution of halophilic bacteria to the red coloration of saltern crystallizer ponds. FEMS Microbiol Ecol 36:123–130PubMedGoogle Scholar
  67. Pathom-aree W, Stach JEM, Ward AC et al (2006) Diversity of actinomycetes isolated from challenger deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10:181–189. CrossRefPubMedGoogle Scholar
  68. Price EP, Sarovich DS, Mayo M et al (2013) Within-host evolution of Burkholderia pseudomallei over a twelve-year chronic carriage infection. MBio 4:e00388-13. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Rodrigues CM, Bio A, Amat F, Vieira N (2011) Artisanal salt production in Aveiro/Portugal—an ecofriendly process. Saline Systems 7:3CrossRefGoogle Scholar
  70. Schlesner H, Lawson PA, Collins MD et al (2001) Filobacillus milensis gen. nov., sp. nov., a new halophilic spore-forming bacterium with Orn-D-Glu-type peptidoglycan. Int J Syst Evol Microbiol 51:425–431CrossRefGoogle Scholar
  71. Schoenafinger G, Marahiel MA (2012) Nonribosomal peptides. In: Civjan N (ed) Natural products in chemical biology, 1st edn. Wiley, Hoboken, pp 111–125Google Scholar
  72. Shin N-R, Roh SW, Kim M-S et al (2012) Knoellia locipacati sp. nov., from soil of the demilitarized zone in South Korea. Int J Syst Evol Microbiol 62:342–346. CrossRefPubMedGoogle Scholar
  73. Siegl A, Hentschel U (2010) PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ Microbiol Rep 2:507–513. CrossRefPubMedGoogle Scholar
  74. Sorokin DY, van Pelt S, Tourova TP, Evtushenko LI (2009) Nitriliruptor alkaliphilus gen. nov., sp. nov., a deeplineage haloalkaliphilic actinobacterium from soda lakes capable of growth on aliphatic nitriles, and proposal of Nitriliruptoraceae fam. nov. and Nitriliruptorales ord. nov. Int J Syst Evol Microbiol 59:248–253. CrossRefPubMedGoogle Scholar
  75. Srinivas TNR, Kumar PA, Tank M et al (2015) Aquipuribacter nitratireducens sp. nov., isolated from a soil sample of a mud volcano. Int J Syst Evol Microbiol 65:2391–2396. CrossRefPubMedGoogle Scholar
  76. Tilton RC (1981) The genus Alcaligenes. In: Starr MP, Stolp H, Trüper HG et al (eds) The prokaryotes: a handbook on habitats, isolation, and identification of bacteria. Springer, Berlin, pp 856–861CrossRefGoogle Scholar
  77. Torres M, Hong K-W, Chong T-M et al (2019) Genomic analyses of two Alteromonas stellipolaris strains reveal traits with potential biotechnological applications. Sci Rep 9:1215. CrossRefPubMedPubMedCentralGoogle Scholar
  78. Tóth EM, Kéki Z, Bohus V et al (2012) Aquipuribacter hungaricus gen. nov., sp. nov., an actinobacterium isolated from the ultrapure water system of a power plant. Int J Syst Evol Microbiol 62:556–562. CrossRefPubMedGoogle Scholar
  79. Tseng CC, Bruner SD, Kohli RM et al (2002) Characterization of the surfactin synthetase C-terminal thioesterase domain as a cyclic depseipeptide synthase. Biochemistry 41:13350–13359. CrossRefPubMedGoogle Scholar
  80. Tsiamis G, Katsaveli K, Ntougias S et al (2008) Prokaryotic community profiles at different operational stages of a Greek solar saltern. Res Microbiol 159:609–627. CrossRefPubMedGoogle Scholar
  81. Van Goethem M, Pierneef R, Bezuidt OKI et al (2018) A reservoir of “historical” antibiotic resistance genes in remote pristine Antarctic soils. Microbiome 6:40CrossRefGoogle Scholar
  82. Van Trappen S, Tan T-L, Samyn E, Vandamme P (2005) Alcaligenes aquatilis sp. nov., a novel bacterium from sediments of the Weser Estuary, Germany, and a salt marsh on Shem Creek in Charleston, USA. Int J Syst Evol Microbiol 55:2571–2575. CrossRefPubMedGoogle Scholar
  83. Vavourakis CD, Ghai R, Rodriguez-Valera F et al (2016) Metagenomic insights into the uncultured diversity and physiology of microbes in four hypersaline soda lake brines. Fron 7:211. CrossRefGoogle Scholar
  84. Ventosa A, Fernández AB, León MJ et al (2014) The Santa Pola saltern as a model for studying the microbiota of hypersaline environments. Extremophiles 18:811–824. CrossRefPubMedGoogle Scholar
  85. Ventosa A, de la Haba RR, Sánchez-Porro C, Papke RT (2015) Microbial diversity of hypersaline environments: a metagenomic approach. Curr Opin Microbiol 25:80–87. CrossRefPubMedGoogle Scholar
  86. Viver T, Cifuentes A, Díaz S et al (2015) Diversity of extremely halophilic cultivable prokaryotes in Mediterranean, Atlantic and Pacific solar salterns: evidence that unexplored sites constitute sources of cultivable novelty. Syst Appl Microbiol 38:266–275. CrossRefPubMedGoogle Scholar
  87. Wang C-Y, Ng C-C, Chen T-W et al (2007) Microbial diversity analysis of former salterns in southern Taiwan by 16S rRNA-based methods. J Basic Microbiol 47:525–533. CrossRefPubMedGoogle Scholar
  88. Wang H, Fewer DP, Holm L et al (2014) Atlas of nonribosomal peptide and polyketide biosynthetic pathways reveals common occurrence of nonmodular enzymes. Proc Natl Acad Sci U S A 111:9259–9264. CrossRefPubMedPubMedCentralGoogle Scholar
  89. Webster NS, Wilson KJ, Blackall LL, Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67:434–444. CrossRefPubMedPubMedCentralGoogle Scholar
  90. Weissman KJ (2009) Introduction to polyketide biosynthesis. Methods Enzymol 459:3–16. CrossRefPubMedGoogle Scholar
  91. Weon H-Y, Kim B-Y, Schumann P et al (2007) Knoellia aerolata sp. nov., isolated from an air sample in Korea. Int J Syst Evol Microbiol 57:2861–2864. CrossRefPubMedGoogle Scholar
  92. Xia J, Xie Z-H, Dunlap CA et al (2017) Rhodohalobacter halophilus gen. nov., sp. nov., a moderately halophilic member of the family Balneolaceae. Int J Syst Evol Microbiol 67:1281–1287. CrossRefPubMedGoogle Scholar
  93. Yoon S-H, Ha S-M, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. CrossRefPubMedPubMedCentralGoogle Scholar
  94. Yu X, Du Y, Wang G (2012) Knoellia flava sp. nov., isolated from pig manure. Int J Syst Evol Microbiol 62:384–389. CrossRefPubMedGoogle Scholar
  95. Zhang J, Du L, Liu F et al (2014) Involvement of both PKS and NRPS in antibacterial activity in Lysobacter enzymogenes OH11. FEMS Microbiol Ecol 355:170–176. CrossRefGoogle Scholar
  96. Zhang J, Ma G, Deng Y et al (2016) Bacterial diversity in Bohai Bay solar saltworks, China. Curr Microbiol 72:55–63. CrossRefPubMedGoogle Scholar
  97. Zhou K, Zhang X, Zhang F, Li Z (2011) Phylogenetically diverse cultivable fungal community and polyketide synthase (PKS), non-ribosomal peptide synthase (NRPS) genes associated with the South China Sea sponges. Microb Ecol 62:644–654. CrossRefPubMedGoogle Scholar
  98. ZoBell CE, Upham HC (1944) A list of marine bacteria including descriptions of sixty new species. Bull Scripps Inst Oceanogr Univ Calif Tech Ser 5:239–292Google Scholar
  99. Zothanpuia PA, Gupta VK, Singh BP (2016) Detection of antibiotic-resistant bacteria endowed with antimicrobial activity from a freshwater lake and their phylogenetic affiliation. PeerJ 4:e2103. CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Biology, Faculty of SciencesUniversity of PortoPortoPortugal
  2. 2.Interdisciplinary Centre of Marine and Environmental ResearchUniversity of PortoMatosinhosPortugal

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